RESEARCH ARTICLE Stroke rates and diving air volumes of … · RESEARCH ARTICLE Stroke rates and diving air volumes of emperor penguins: implications for dive performance Katsufumi

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INTRODUCTIONThe concept of an aerobic dive limit (ADL) emphasizes theefficiency of aerobic energy production as the metabolic basis forthe performance of routine, frequent, repetitive dives to depth(Kooyman et al., 1983; Kooyman et al., 1980). Defined as the diveduration associated with the onset of post-dive lactate accumulation,the ADL has become fundamental to the interpretation of divingphysiology, dive behavior and foraging ecology (Butler and Jones,1997; Kooyman and Ponganis, 1998). Dives beyond the ADL areless frequent and are associated with prolonged surface intervals,presumably because of the recovery period required after longduration dives.

However, emperor penguins (Aptenodytes forsteri, Gray 1844),both at sea and at an isolated experimental dive hole (Kooyman andKooyman, 1995; Ponganis et al., 2007), routinely dive beyond the5.6min measured ADL (ADLM) determined by post-dive bloodlactate analyses in emperor penguins diving at an isolated dive hole(Ponganis et al., 1997b). In addition, surface intervals after diveseven as long as 10min are often less than 1–2min in both situations(Ponganis et al., 2007; Wienecke et al., 2007). Such repetitive divingability beyond the ADLM raises questions about the duration of

aerobic metabolism during individual dives of emperor penguins,the post-dive metabolism of lactate, anaerobic capacity, and thetolerance of high lactate levels in these birds.

To address this remarkable capacity for long dives in emperorpenguins, we applied dive recorders (depth, speed, 2-D acceleration)to emperor penguins diving at the isolated dive hole and to emperorpenguins making foraging trips to sea from the Cape Washingtoncolony in Antarctica. First, we wanted to evaluate the relationshipof surface interval to dive duration, especially at the isolated divehole. We wished to determine whether prolongation of minimumsurface intervals occurred near the 5.6min ADLM. Second, wehypothesized that stroke rates for dives of given duration were lowerat sea than at the isolated dive hole. Because an at-sea behavioralADL (ADLB) of 8min had previously been estimated on the basisof a prolongation of post-dive intervals (Kooyman and Kooyman,1995), we postulated that stroke rate, an index of muscle workloadand the depletion rate of the muscle O2 store, would be 40% lowerat sea. Such a reduction in stroke rate could account for the 2.4-min difference between the ADLB at sea and the ADLM at theisolated dive hole as well as for the relatively short surface intervalsafter long dives at sea. Third, we hypothesized that the magnitude

The Journal of Experimental Biology 214, 2854-2863© 2011. Published by The Company of Biologists Ltddoi:10.1242/jeb.055723

RESEARCH ARTICLE

Stroke rates and diving air volumes of emperor penguins: implications for diveperformance

Katsufumi Sato1,*, Kozue Shiomi1,*, Greg Marshall2, Gerald L. Kooyman3 and Paul J. Ponganis3,†

1International Coastal Research Center, Atmosphere and Ocean Research Institute, The University of Tokyo, 2-106-1, Akahama,Otsuchi, Iwate, 028-1102, Japan, 2National Geographic – Remote Imaging, 1145 17th Street NW, Washington, DC 20036, USA and3Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla,

CA 92093-0204, USA*Present address: International Coastal Research Center, Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5

Kashiwanoha, Kashiwa, Chiba, 277-8564, Japan†Author for correspondence ([email protected])

Accepted 22 May 2011

SUMMARYEmperor penguins (Aptenodytes forsteri), both at sea and at an experimental dive hole, often have minimal surface periods evenafter performance of dives far beyond their measured 5.6min aerobic dive limit (ADL: dive duration associated with the onset ofpost-dive blood lactate accumulation). Accelerometer-based data loggers were attached to emperor penguins diving in these twodifferent situations to further evaluate the capacity of these birds to perform such dives without any apparent prolonged recoveryperiods. Minimum surface intervals for dives as long as 10min were less than 1min at both sites. Stroke rates for dives at seawere significantly greater than those for dives at the isolated dive hole. Calculated diving air volumes at sea were variable,increased with maximum depth of dive to a depth of 250m, and decreased for deeper dives. It is hypothesized that lower airvolumes for the deepest dives are the result of exhalation of air underwater. Mean maximal air volumes for deep dives at sea wereapproximately 83% greater than those during shallow (<50m) dives. We conclude that (a) dives beyond the 5.6min ADL do notalways require prolongation of surface intervals in emperor penguins, (b) stroke rate at sea is greater than at the isolated dive holeand, therefore, a reduction in muscle stroke rate does not extend the duration of aerobic metabolism during dives at sea, and (c)a larger diving air volume facilitates performance of deep dives by increasing the total body O2 store to 68ml O2kg–1. Althoughincreased O2 storage and cardiovascular adjustments presumably optimize aerobic metabolism during dives, enhanced anaerobiccapacity and hypoxemic tolerance are also essential for longer dives. This was exemplified by a 27.6min dive, after which the birdrequired 6min before it stood up from a prone position, another 20min before it began to walk, and 8.4h before it dived again.

Key words: aerobic dive limit, diving air volume, emperor penguin, oxygen stores, stroke rate, surface interval.

THE JOURNAL OF EXPERIMENTAL BIOLOGY

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of the respiratory O2 store was greater during deep dives than duringshallow dives of emperor penguins. Increased air volumes duringdeep dives had previously been observed in both king (A.patagonicus) and Adélie (Pygoscelis adeliae) penguins (Sato et al.,2002). Because the ADLM was determined during shallow divingat the isolated dive hole (Ponganis et al., 1997b), such an increasein the respiratory O2 store during deep dives could contribute toprolonged aerobic metabolism during long, deep dives at sea. Anincrease in the respiratory O2 store might then contribute to therepetitive diving ability of emperor penguins at sea and to thedifferences between the ADLB at sea and the ADLM at the isolateddive hole.

MATERIALS AND METHODSField studies

The first field study was conducted in McMurdo Sound, Antarcticaduring the period from 14 November to 4 December 2004. Threeemperor penguins, ranging from 24.4 to 27.4kg, were captured nearthe sea ice edge of eastern McMurdo Sound. They were maintainedin a corral at a research camp (Penguin Ranch) on the McMurdosea ice (77°43�S, 166°07�E). The penguins foraged daily beneaththe sea ice with entry and exit through two 1.2m wide dive holesdrilled inside the corral. A data logger was attached to the centralback of each penguin with waterproof TesaTM tape (Beiersdorf AG,Hamburg, Germany) and glue (Loctite epoxy, Henkel, Westlake,OH, USA) while the bird was under hand restraint. The bird wasallowed to dive, and the data logger was retrieved 38–60h afterattachment. Each bird was instrumented one to three times.

The second field study was conducted at the breeding colony atCape Washington (74°39�S, 165°24�E) during the chick-rearingperiod from 26 October to 24 November 2005. All deployments ofdata loggers were conducted on 28 October. Fourteen birds departingfor foraging trips were captured at the edge of the colony. Dataloggers were attached to the central back feathers using waterprooftape and stainless steel cable ties. VHF transmitters (Model MM130,ATS, Isanti, MN, USA) were attached to the lower back with cableties. Body mass was measured to the nearest 100g at deploymentand recapture, using a balance (Pesola 50kg). After release, everybird walked toward open water. Handling time was less than 30min.

Instruments3-D loggers (W1000L-3MPD3GT, Little Leonardo Ltd, Tokyo,Japan) were used for the first field study at the isolated dive hole.The W1000-3MPD3GT was 26mm in diameter, 174mm in length,had a mass of 120g in air, and recorded 3-axes magnetism (1Hz),speed (1Hz), depth (1Hz), temperature (1Hz) and 3-axesacceleration (either 16 or 32Hz for each deployment). These dataallowed construction of underwater 3-D dive paths (Shiomi et al.,2008); however, only dive parameters, such as dive depth andduration, swim speed and stroke rate were used in the present study.Acceleration data loggers (W1000L-PD2GT and W1000L-PD2GT,Little Leonardo Ltd) and 3-D loggers (W1000L-3MPD3GT, LittleLeonardo Ltd) were used for the second field study to obtain detailedinformation at sea (depth, speed and acceleration) during theforaging trip. In the second field study, nine W1000-PD2GT wereused and data were obtained from seven of them. The W1000-PD2GT was 22mm in diameter, 122mm in length, had a mass of73g in air, and recorded speed (1Hz), depth (1Hz), temperature(1Hz) and 2-axes accelerations (16Hz). The devices were set tostart recording 4–96h (4 days) after deployment (Table1). Datalength of W1000-PD2GT ranged from 3.9 to 4.1 days (Table1).Two W1000L-PD2GT (capacity of memory was larger than W1000-

PD2GT) were used and data were obtained from them. TheW1000L-PD2GT was 27mm in diameter, 128mm in length, had amass of 101g in air, and recorded speed (1Hz), depth (1Hz),temperature (1Hz) and 2-axes acceleration (16Hz). Data lengths ofthe W1000L-PD2GT were 14.3 and 14.5 days (Table1). ThreeW1000L-3MPD3GT (3-D logger) were used and data were obtainedfrom one of them at sea. Data length of W1000L-3MPD3GT was11.5 days, which covered the whole foraging trip.

Loggers were positioned so as to detect longitudinal and dorso-ventral acceleration. In this paper, 3-axes magnetism is notconsidered. Acceleration output values from the recorders wereconverted into acceleration (ms–2) with linear regression equations.To obtain the calibration equations, values recorded by each sensorat 90 and –90deg from the horizontal were regressed on thecorresponding acceleration (9.8 and –9.8ms–2, respectively).Loggers measured both specific acceleration (such as wing strokingactivity) and gravity-related acceleration. Low-frequencycomponents (<0.5Hz) of the fluctuation in longitudinal acceleration,along the long axis of the body, were used to calculate the pitchangle of the animal (Sato et al., 2003). The depth criterion for adive was 1m.

To test the effect of dive depth on dive duration, linear mixedmodels were fitted with dive duration as a response variable, divedepth as a fixed effect, and individual as a random effect at eachstudy site (at sea and at the isolated dive hole). Then, to test theeffect of site on slope, two generalized linear mixed models werefitted with Poisson error distribution and a logarithm link function,in which dive duration was a response variable with dive depth asan offset term, and individual as a random effect. One modelincluded place (at the isolated dive hole or at sea) as a fixed effect,the other did not. Akaike information criteria (AIC) were used toselect the most parsimonious model. For the model fitting, R 2.10(R Development Core Team, 2009) was used with glmer functionin R package lme4 (Bates and Maechler, 2009).

Stroke rate analysisIn order to examine the difference in stroke rate between birds atthe isolated dive hole and birds foraging at sea, the number of strokesduring a dive was calculated with the longitudinal acceleration data,in which stroking activities were presented as regular peaks (Satoet al., 2005; van Dam et al., 2002). Then, two types of generalizedlinear mixed models were fitted with Poisson error distribution anda logarithm link function, in which the total number of strokes duringa dive was a response variable with dive duration as an offset termand individual as a random effect. One model included place (atthe isolated dive hole or at sea) as a fixed effect, the other did not.AIC were compared between the two fitted models. For the modelfitting, R 2.10 (R Development Core Team, 2009) was used withglmer function in R package lme4 (Bates and Maechler, 2009).

Diving air volume analysisSwim speed during the prolonged glide period during final ascentwas used to estimate diving air volume in dives at sea followingthe methods of a previous study (Sato et al., 2002). The diving airvolumes were estimated for dives selected at random (N425 divesby 10 birds). Using the biomechanical model (Sato et al., 2002),the model simulation was conducted for each dive under severalvalues of air volume. The simulated speeds were then comparedwith the measured speed to select an appropriate value of the airvolume for each dive. The estimated air volume was compared withdive depth. To test the effect of dive depth on the estimated airvolume, both a linear mixed model and a quadric mixed model were


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fitted with diving air volume as a response variable, dive depth asa fixed effect, and individual as a random effect. AIC was used toselect the most parsimonious model from the model includingrandom effect only, the linear mixed model and the quadric mixedmodel. For the model fitting, R 2.10 (R Development Core Team,2009) with glmer function in R package lme4 (Bates and Maechler,2009) and Matlab (MathWorks, Natick, MA, USA) with nlmefitfunction were used.

RESULTSCape Washington deployments

Measured masses of the Cape Washington birds were between 21.5and 29.0kg, in the same range as those of the penguins(24.4–27.4kg) at the isolated dive hole (Table1). Two of the 14birds were recaptured near the colony 3 days later. The two birdsseemed to be non-breeding birds because they did not depart forthe foraging trip and wandered around the colony. Another birdwas not recaptured because it was never relocated. The other 11birds were recaptured at the colony and the instruments wereretrieved. One of the 11 instruments did not work because ofmechanical trouble. Data were obtained from the other 10 birds.According to the body mass measurements, net mass gain rangedfrom 0.5 to 5.0kg (N10 birds) (Table1) after foraging tripdurations of 7.9 to 19.7 days. Small mass gains (0.5kg) might besecondary to feeding of chicks prior to recapture. We succeededin recapturing two birds on the way back to the colony. Their massgains were both 2.5kg.

K. Sato and others

General description of divesAll 10 birds at sea performed dives during the sampling periods oftheir recorders. Mean dive duration ranged from 1.7 to 2.9min, andthe maximum dive duration was 27.6min (CW8, Table2), whichis now the longest recorded dive of any avian diver. The maximumdive depth for each bird ranged from 357.5 to 513.5m, and meandive depths were between 28.3 and 71.9m. Mean dive durationsfor three birds at the isolated dive hole ranged from 1.8 to 3.0min,similar to those of free-ranging birds at sea, but mean dive depthsat the isolated dive hole were between 13.0 and 15.8m, and themaximum dive depth of each bird was shallower than 100m(Table2). According to the histograms in Fig.1A, most dives at seawere also shallower than 100m; however, 18.3% of dives weredeeper than 100m. Most dives at sea and at the isolated dive holewere shorter than 10min (99.7 and 92.3% were ≤10min,respectively; Fig.1C,D).

Dive duration increased with dive depth at sea (Fig.2A). AICof the model with dive depth as a fixed effect (AIC: 235,995)was smaller than that of the model including a random effect only(AIC: 259,668). However, dive duration of shallow dives variedconsiderably (Fig.2A). Some shallow dives at sea were long, andthe extreme long dives (>10min) were shallow, near 100m(Fig.2A). The longest recorded dive duration (27min 36s) of thisspecies was attained in a shallow dive of 110m by a free-rangingbird (CW8) at sea. There was also a positive relationship betweendive depth and dive duration at the isolated dive hole. AIC of themodel with dive depth as a fixed effect (AIC: 23,463) was smaller

Table 1. Field study of emperor penguins at a breeding colony in Cape Washington

Logger Delay time Initial body mass Place and status Final body mass Mass gain Trip duration Data length ID (kg) (h) (kg) when recaptured (kg) (kg) (days) (days)

CW1 W1000-PD2GT 8 29.0 In colony No data No data 7.9 4.0 CW2 W1000-PD2GT 8 23.0 On the way to the colony 25.5 2.5 10.0 4.1 CW3 W1000-PD2GT 8 21.5 In colony 25.5 4.0 17.8 4.1 CW4 W1000-PD2GT 48 23.5 In colony 25.5 2.0 13.5 3.9 CW7 W1000-PD2GT 96 24.0 On the way to the colony 26.5 2.5 16.1 4.0 CW8 W1000-PD2GT 96 27.5 In colony 30.5 3.0 13.7 3.9 CW9 W1000-PD2GT 96 24.0 In colony with chick 26.5 2.5 15.0 4.0 CW10 W1000L-PD2GT 4 25.5 In colony 30.5 5.0 19.7 14.3 CW11 W1000L-PD2GT 4 22.0 In colony with chick 22.5 0.5 16.5 14.5 CW13 W1000L-3MPD3GT 4 26.0 In colony 30.0 4.0 11.5 11.5

Table 2. Diving characteristics of emperor penguins at sea (Cape Washington) and the isolated dive hole (Penguin Ranch)

Dive duration (min) Dive depth (m)

ID N Mean ± s.d. Max. Mean ± s.d. Max.

Cape WashingtonCW1 906 2.0±1.9 8.4 28.3±48.8 357.5 CW2 1479 1.7±2.5 12.2 42.8±78.7 418.0 CW3 1153 2.0±2.3 12.7 38.4±55.9 423.0 CW4 1264 2.1±2.5 11.5 39.1±74.4 513.5 CW7 1376 2.1±2.5 12.5 49.6±95.0 475.8 CW8 1167 2.0±2.5 27.6 38.2±78.4 501.8 CW9 953 2.8±2.7 10.9 68.3±101.7 499.5 CW10 3447 2.9±2.3 12.1 71.9±76.1 458.8 CW11 5859 1.7±2.1 12.7 30.6±50.1 400.3 CW13 2959 2.6±2.4 17.3 43.3±68.2 509.2 Total 20430 2.2±2.4 – 44.8±71.4 –

Penguin RanchPR1 420 3.0±4.3 19.8 15.8±16.7 80.3 PR2 1213 1.8±3.9 19.1 13.0±15.6 95.8 PR3 274 2.7±5.1 22.1 14.7±17.4 69.8 Total 1907 2.0±3.9 – 13.5±16.5 –



than that of the model including a random effect only (AIC:26,193). AIC of the model with place (at the isolated dive holeor at sea) as a fixed effect was smaller than that of the model notconsidering place as an effect (AIC: 965,921 and 965,943,respectively). Birds at the isolated ice hole also performedshallow, long dives (Fig.2B).

Surface interval analysisSurface intervals varied considerably for any given dive durationboth at sea and at the isolated dive hole (Fig.3A,B). Minimumsurface intervals were less than 1min even after dives as long as10min at both sites. There was no apparent distinct inflectionpoint toward longer surface intervals. After classification of divesof <2min or <50m as part of the post-dive interval at sea(Kooyman and Kooyman, 1995), re-analysis demonstrated thatthe minimum post-dive interval began to increase above 1minafter dives of 6–7min duration (Fig.3C). The minimum post-diveinterval was near 2min at dive durations of 9–10min except fortwo points (Fig.3C). Similar analysis of post-dive intervals atthe isolated dive hole with a filtering criterion of dives <2minsuggested that minimum post-dive interval began to increaseabove 1min at dive durations of 6–7min (Fig.3D). However, asat sea, there were dives of >10min duration with post-diveintervals less than 2min (Fig.3D).

Stroke rateThe total number of strokes per dive increased with dive durationat both sites (Fig.4). AIC of the model with place as a fixed effectwas smaller than that for the model not considering place as aneffect (AIC: 65,997 and 66,003, respectively). The estimated slope(calculated as number of strokess–1) was smaller for birds at theisolated dive hole than for free-ranging birds at sea (0.38 and 0.59,respectively), which means that stroke rates were different betweensites and were less for birds diving at the isolated dive hole.

Detailed behavior of the longest diveFig.5 illustrates the entire data record of the longest reported diveby a 27.5kg emperor penguin (CW8). The bird reached a maximumdepth of 110m and then swam at depths ranging between 30 and60m. Mean swim speed in the descent phase was 2.1±0.1ms–1; meanswim speed decreased to 1.7±0.3ms–1 during the later, shallower

portion of the dive. The penguin adopted a stroke-and-glide methodduring most of the dive, and stopped flipper beating during the finalascent at a depth of 48m, after which it glided up to the sea surfacein 37s (Fig.5B). Swim speed increased from 1.5 to 3.1ms–1 duringthe passive ascent period. After this longest dive of 27.6min, the

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penguin remained in a prone position (lying horizontal on itsabdomen) for 5.9min (Fig.5C), and then stood quietly (pitch70–80deg) for 20min. During the initial prone position, periodicmovements were apparent in both dorso-ventral acceleration andpitch angle (Fig.5C). We assume these movements are indicativeof breathing. The overall respiration rate during the 5.9min post-dive prone period was 17.8breathsmin–1. The respiratory rate was22breathsmin–1 during the first minute; it gradually decreased over2.5min to 15breathsmin–1 (Fig.5C).

Diving air volumeAll penguins at sea stopped stroking during ascent and madeprolonged glides to the surface. Durations of the prolonged glideswere relatively short, less than 9% of dive durations. Examplesof the swim speed simulation results for passive ascents ofshallow and deep dives are shown in Fig.6. The calculated speedsunder the conditions of 1.6 and 4.2l diving air volume (at 1atmpressure, ~101kPa) accorded well with the measured speeds ofthe shallow (43.3m) and deep (411.3m) dives, respectively(Fig.6). They indicate that the penguin could ascend passively atthe recorded speeds if 1.6 and 4.2l of air, respectively, wereretained in the body.

The estimated air volumes of shallow dives were small. Airvolume increased with dive depth up to 250–300m and decreasedin deep dives of 400–500m (Fig.7). AIC of the quadric mixed model(V–0.0009D2+0.4396D+63.5482, AIC: 3832) was smaller than thatof the model including random effect only (AIC: 4010) and the linearmixed model (V0.02861D+89.56698, AIC: 4007), where V isdiving air volume (mlkg–1) and D is dive depth (m).

K. Sato and others

The calculated diving air volume is the volume of air in the bodyduring the final phase of each dive. That value has been assumedto reflect the inspiratory air volume at the start of the dive (Sato etal., 2002). However, variation in the magnitude of air volumes duringthe final ascent may at least in part be the result of exhalation of

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air during the dive prior to the glide phase of the ascent. To examinethis possibility, the initial descent stroking pattern of one bird wasused as a relative index of inspiratory air volume. At the same swimspeed, stroke effort should be proportional to buoyancy, and, hence,the inspiratory air volume. Fig.8 illustrates the initial strokingpatterns of a 23.0kg penguin (CW2) in the first 10s of four dives.Each example (Fig.8A–D) corresponds with the points indicated inFig.7. In the case of a shallow dive with a small estimated air volume(Fig.8A), stroke rate was 1.1Hz at the beginning of the dive. Thedive in Fig.8B was also shallow, but both estimated diving airvolume (4.3l) and initial stroke rate (1.7Hz) were high while swimspeed was low in this dive. In the case of deep dives (Fig.8C,D),estimated air volumes were 3.5 and 1.6l; however, initial stroke

rates were 1.7 and 1.9Hz, respectively (Fig.8C,D), implying thatthe inspiratory air volume in the dive shown in Fig.8D may havebeen greater than that calculated during the final ascent. Such adifference may be the result of exhalation of air during the diveprior to the gliding ascent. Such exhalations may account for the40–170mlkg–1 range of estimated diving air volumes of deep dives(>300m) (Fig.7).

DISCUSSIONDive behavior

Maximum depths of dive and dive durations of emperor penguinsduring foraging trips to sea (Table2, Fig.1) were similar to thoseobtained in previous studies during foraging trips to sea in the chick-rearing period (Kirkwoods, 2001; Kirkwood and Robertson, 1997;Kooyman and Kooyman, 1995; Robertson, 1995). Of note is thelongest recorded dive of an emperor penguin to date; a 27.6mindive by CW8. Although maximum dive depths were generallyshallower at the isolated dive hole, the distribution of dive durationswas shifted towards longer dives (Figs1 and 2). The shallow divesat the isolated dive hole are a consequence of the availability andhunting of prey fish beneath the surface of the sea ice (Ponganis etal., 2000). At the isolated dive hole, 12.6% of dives were >5.6min(ADLM), and 10.3% were >8min (ADLB).

It is remarkable that emperor penguins foraging from CapeWashington (this study) and Coulman Island (Kooyman andKooyman, 1995) dive to depths >400m much more routinely thanthose diving in East Antarctica (Wienecke et al., 2007). In 137,364dives by 93 penguins in East Antarctica, only 15 birds performeddives >400m, and only one dived deeper than 500m. In contrast,in our study, 9 of 10 birds dived deeper than 400m, and three birdsdived >500m.

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Fig.6. Relationship between measured swim speed (thick black line) andsimulated speed (colored lines) during the passive ascent periods of dives155 (A) and 612 (B) of an emperor penguin (CW2). Values beside thecolored lines are diving air volumes (at 1atm, ~101kPa) used in the modelsimulation. The depths at which the bird stopped flipper beating areindicated in parentheses.


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The relationship of dive duration to maximum depth of diveduring foraging trips to sea was also similar to that in prior studiesof foraging emperor penguins (Fig.2A). If one considers that dives<2min or <50m are probably not foraging dives at sea (Kooymanand Kooyman, 1995), the majority of foraging dives at sea arebetween 5 and 10min, and 50–500m (Fig.2A). Dives longer than5.6min (ADLM) were 10.1% of all dives or a ~2100 dives; divesgreater than 8min (ADLB) in duration were 1.9% of all dives(approximately 400 dives).

Surface interval–dive duration relationshipsExamination of the surface interval to dive duration relationshipboth at sea and at the isolated dive hole demonstrated that minimumsurface interval did not increase for dives beyond the ADLM

(Fig.3A,B). It is possible that prolongation of surface intervals onlyoccurs after a much greater lactate accumulation than that necessaryfor detection of an initial small elevation of post-dive blood lactate(the ADLM) (Kooyman and Kooyman, 1995; Ponganis et al., 1997b).As demonstrated previously in both Weddell seals (Leptonychotesweddellii) and Baikal seals (Phoca sibirica), animals can have shortsurface intervals and continue to dive despite elevated blood lactateconcentrations; in addition, elevated blood lactate concentrationscan decrease during the breath-hold period (Castellini et al., 1988;Ponganis et al., 1997a). The relatively rapid decline measured inpost-dive blood lactate concentrations of emperor penguins wouldalso facilitate repetitive diving activity (Ponganis et al., 1997b).

The surface interval and dive duration data were also filtered toobtain post-dive interval. In this process (Kooyman and Kooyman,1995), dives at sea were considered recovery dives and, therefore,part of the post-dive interval if the dives were <2min in durationor <50m in depth. Because most dives at the isolated dive hole wereshallow, only dives <2min in duration were considered recoverydives. After such data processing (Fig.3C,D), minimum post-diveinterval increased above 1min after dives of 6–7min duration bothat the isolated dive hole and at sea, i.e. in the general range of thepreviously determined 5.6min ADLM and 8min ADLB. For divedurations of 10min, the minimum post-dive interval was near 2min.Thus, in our study, for 99.7% of all dives at sea, and 92.5% of dives

K. Sato and others

at the isolated dive hole (i.e. those under 10min dive duration), theminimum post-dive intervals were less than 2min.

From these minimum surface interval and minimum post-diveperiod analyses, it appears that emperor penguins can successfullyperform many dives at sea without the need for an extended surfaceinterval or even an extended post-dive period. This is similar toprevious analyses of long and deep dives of emperor penguins divingin East Antarctica (Wienecke et al., 2007). Indeed, most minimumsurface intervals are ≤1min, the mean time for replenishment ofblood and air sac O2 stores (Ponganis et al., 2009). Thus, recoveryfrom any elevation in blood lactate concentration is either rapid ordoes not always require a significant increase in the post-diveinterval. Conversely, different physiological responses duringdifferent types of dive may prolong the duration of aerobicmetabolism and delay the onset of lactate accumulation.

Stroke rateA lower stroke rate at sea than at the isolated dive hole is onemechanism that could account for a longer ADL at sea and for theperformance of repetitive, long deep dives at sea. However, in contrastto this hypothesis, stroke rates of dives at sea were actually greaterthan those of dives at the isolated dive hole (Fig.4). This wasunexpected because dives of penguins at sea typically have a periodof prolonged gliding during ascent (Sato et al., 2002) whereasprolonged gliding does not occur during dives at the isolated divehole (van Dam et al., 2002) (present study). Despite this lack ofprolonged gliding, the total number of strokes per dive at the isolateddive hole was less than that for a dive of similar duration at sea (Fig.4).

0 100 200 300 400 500D (m)

V (

ml k

g–1 )

200

160

120

80

40

0

B

A

C

D

Fig.7. Relationship between dive depth (D) and estimated air volume (V) of10 emperor penguins (N425). Thick red curve indicates the mostparsimonious model selected by mixed model analysis(V–0.0009D2+0.4396D+63.5482). Letters A–D indicate values used inFig.8.

A Dive depth 43 m, air volume 1.6 l, swim speed 2.2 m s–1,

mean stroke rate 1.1 Hz

B Dive depth 39 m, air volume 4.3 l, swim speed 1.2 m s–1,


C Dive depth 383 m, air volume 3.5 l, swim speed 1.5 m s–1,


D Dive depth 384 m, air volume 1.6 l, swim speed 1.5 m s–1,


0 2 4 6 8 10Elapsed time from the beginning of dive (s)

Dor

so-v

entr

al a

ccel

erat

ion

(m s

–2)

0

5

10

15

0

5

10

15

0

5

10

15

0

5

10

15

Fig.8. Stroking patterns in the first 10s of dives by an emperor penguin(CW2). (A)A shallow dive with a low calculated diving air volume, (B) ashallow dive with a large air volume, (C) a deep dive with a larger airvolume, and (D) a deep dive with a small calculated air volume. Strokerates were 1.1, 1.7, 1.7 and 1.9Hz in dives A–D, respectively. The lettersA–D correspond to the dives with the marked air volumes A–D in Fig.7.



Assuming stroke rate is an adequate index of muscle workload andmetabolic rate (Williams et al., 2000; Williams et al., 2004), muscleO2 consumption is greater at sea than at the isolated dive hole. Basedupon the mean number of strokes for dives at sea, stroke rate andmuscle workload are about 1.6 times greater than those for dives ofsimilar duration at the isolated dive hole. If the onset of post-divelactate accumulation were solely dependent on the depletion of amuscle O2 store isolated from the circulation, the ADLM at sea wouldbe less than at the isolated dive hole. Our hypothesis that a decreasedstroke rate and muscle workload at sea could account for a longerADL (behavioral or measured) at sea is not correct. For birds at theisolated dive hole, we suspect that the shift towards longer durationsof dives (Fig.1) is supported by a lower diving metabolic rate affordedby the lower stroke rates and muscle workloads (Fig.4) as well as bythe extreme bradycardias during these dives (Meir et al., 2008). Itshould also be noted that we have assumed that stroke rate is anadequate index of muscle workload. It is possible that stroke thrustand amplitude may vary with individual strokes, and also contributeto muscle workload (Williams et al., 2011). These parameters awaitfurther investigation.

Diving air volumeDiving air volume was estimated on the basis of body angle andswim speed during the prolonged gliding phase of the final ascentof a dive. As explained previously (Sato et al., 2002), and againreviewed in Fig.6, this is the volume of air at surface air pressure,which, when compressed at depth, converted to buoyancy andcombined with body angle, can best approximate the swim speedprofile observed during the gliding ascent. Penguins do not appearto exhale during most of this gliding ascent because the observedspeed profile should otherwise shift to that predicted by a lesser airvolume. Such a shift in swim speed as evidence for exhalation ofair or for other breaking maneuvers only occurs during the last 3–7sof the ascent (Fig.6). Exhalations at the end of ascent have beenobserved in penguins at sea (G.L.K. and P.J.P., unpublishedobservations). Consequently, the calculated air volume is consideredto be the air volume (corrected to surface air pressure) that is in thebody during that portion of the gliding ascent during which theobserved swim speeds follow the predicted profile (i.e. prior to thoselast 3–7s of the ascent).

Provided the bird does not exhale or otherwise lose air earlier inthe dive (i.e. prior to the start of the gliding ascent), this calculatedair volume should be representative of the initial air volume at thestart of a dive. If the bird does exhale prior to the start of the glidingascent, the initial start-of-dive air volume would be underestimatedby this calculation. Note also that the calculated diving air volumeincludes both plumage air and respiratory air (lungs and air sacs).Loss of plumage air during a dive prior to the gliding ascent mayalso contribute to a lower-than-expected calculated diving airvolume. However, plumage air is only about 10% of the diving airvolume in simulated dives under restraint conditions, and diving airvolumes of simulated dives appear to be at the low end of the range

of diving air volumes at sea (Kooyman et al., 1973; Sato et al.,2002; Sato et al., 2006). Consequently, with these caveats in mindand as in past papers, the entire diving air volume will be used forrespiratory oxygen store calculations in this paper.

Diving air volume of emperor penguins increased with maximumdepth of dive to about 200–300m depth (Fig.7). An increase in theestimated diving air volume with maximum depth is consistent withdata from other penguin species (Sato et al., 2002). However, unlikein other penguin species, there was a decrease in diving air volumefor dives at greater depths (especially between 400 and 500m depth).This decline may be consistent with air volumes at the start of thesedeepest dives that are lower than those of the 200–300m deep dives.The values for these deepest dives are closer to those for the divesof less than 100m (Fig.7).

However, the low values for 400–500m deep dives in Fig.7suggest to us that the birds may be exhaling prior to the start of thegliding ascent during these very deep dives. Indeed, the variationin diving air volumes at all depths (Fig.7) may be due either to useof different inspiratory air volumes during dives to the same depthand/or to exhalation of air prior to the start of the gliding ascentsduring all dives. Such exhalations may affect maneuverability, speedand hunting strategy. Weddell seals, for example, have beenobserved to flush fish out of the sub-ice platelet layer withexhalations (Davis et al., 1999). Exhalation of air has also beenreported during early ascents of Antarctic fur seals (Arctocephalusgazella) (Hooker et al., 2005).

To assess the possibility of exhalation of air prior to the glidingascent, initial stroke rates during dives were examined in one bird(Fig.8). Interpretation of initial stroke rates during dives in Fig.8is dependent on the assumption that those values are a relative indexof buoyancy and, hence, initial diving air volume (see Materialsand methods). For the shallow dives in Fig.8A and B, the differencein initial stroke rate supports the dive volume calculation, andsuggests that even for shallow dives, there may be a wide range ofinspiratory volumes. The high stroke rate during the deep dive inFig.8C was also consistent with the dive volume calculation andsupported the hypothesis that inspiratory air volumes are large fordeep dives. For the deep dive in Fig.8D, the high stroke rate, butlow calculated air volume suggest that the bird dived with a largeinspiratory air volume (high stroke rate), but that the bird exhaledduring the dive prior to the ascent, the time for which the air volumewas calculated. Therefore, although initial diving air volume isvariable for a given depth, we think that inspiratory air volumegenerally increases with depth of dive and is even elevated for divesto 500m. We attribute the inverted U-shaped relationship of divingair volume to maximum dive depth to exhalation of air prior to thestart of the gliding ascent during the deepest dives. In addition, thevariability in the air volume data at all depths may be at least partiallysecondary to such exhalations. Possible exhalation of air representsa limitation of the use of diving air volume to estimate inspiratoryair volume. Evaluation of this possibility awaits future applicationof animal-borne camera technology to emperor penguins at sea.

Table 3. Magnitude and distribution of oxygen stores in penguins

Oxygen store (mlkg–1)

Dive type Respiratory volume (mlkg–1) Air Blood Muscle Total

Shallow dives 64 12.2 21.1 24.4 57.7 Deep dives 117 22.2 21.1 24.4 67.7

The maximum respiratory oxygen extraction during a dive was assumed to be 19% (Ponganis et al., 2010). Respiratory volumes are calculated as described inMaterials and methods.


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If we assume the mean values of calculated diving air volumes inFig.7 are representative of the initial diving air volume, then theinspiratory air volumes of 200–400m deep dives are near 117mlkg–1

(Fig.7). Given the possible early exhalation of air during a dive andthe subsequent potential limitations of these estimations, it isremarkable that this mean value is 98% of the mean respiratorycapacity (120±2mlkg–1) predicted for the body masses of thesepenguins by an allometric equation (Lasiewski and Calder, 1971).Maximum diving air volumes of king and Adélie penguins are alsoin the same range as those predicted by the allometric equation (Satoet al., 2002). These findings reinforce the concept that penguins diveon inspiration. However, given the variability in data (the highestvalues near 160mlkg–1 in Fig.7), and the possibility of air exhalation,this mean value may underestimate the true start-of-dive air volume.Nonetheless, at this time, this 117mlkg–1 value appears to be the bestavailable estimate of the inspiratory air volume for deep dives.

Based on this analysis of the diving air volume data, mean initialair volumes of emperor penguins increase significantly from 64 to117mlkg–1 between shallow dives (<50m) and deep dives(100–400m). The former is the mean diving air volume of thequadric model for the shallowest dives; the latter is the maximumvalue of the quadric model. The shallow dive value is similar to themean 69mlkg–1 value measured in king penguins during simulateddives (Ponganis et al., 1999). The difference in diving air volumesbetween shallow and deep dives at sea represents an 83% increasein the size of the respiratory O2 store (Table3).

Respiratory and total body O2 storesWith 19% maximum respiratory O2 extraction during a dive(Ponganis et al., 2010), and diving air volumes of 64 and 117mlkg–1

for shallow and deep dives, respectively, the available mass-specificrespiratory O2 store ranges from 12.2 to 22.2ml O2kg–1 during divesof emperor penguins at sea. Use of the previous 69mlkg–1 air volumeof king penguins during simulated dives (Ponganis et al., 1999) anda 19% O2 extraction, yields a respiratory O2 store of 13.1ml O2kg–1

(Ponganis et al., 2010). Thus, the maximum respiratory O2 storeresulting from larger diving air volumes in deep dives is 69% greaterthan past estimates based on air volumes during simulated divestudies.

With these estimates of respiratory O2 stores, total body O2 storescan be calculated for deep and shallow dives of emperor penguins.Given the new estimates of blood O2 extraction and the differentialdistribution of myoglobin in the pectoralis–supracoracoideusmuscles versus other muscles in the body (Ponganis et al., 2010),current best calculations of the mass-specific blood and muscle O2

stores in emperor penguins are 21.1 and 24.4ml O2kg–1,respectively. These results and the 22.2ml O2kg–1 respiratory O2

store for deep dives yield a total body O2 store of 68 (67.7)mlO2kg–1, with 33, 31 and 36% of O2 in the respiratory system, bloodand muscle, respectively, for a diving air volume of 117mlkg–1. Incontrast, for a diving air volume of 64mlkg–1, the total body O2

store is 58 (57.7)ml O2kg–1, with 21, 37 and 42% of O2 in therespiratory system, blood and muscle, respectively.

In addition to a difference in the magnitude of the body O2 storesduring different types of dive, we suspect that emperor penguinsexhibit a spectrum of cardiovascular responses dependent on thenature and depth of a dive. Variable rates of air sac and blood O2

depletion and highly variable venous PO2 and Hb saturation profilesin dives at the isolated dive hole have all suggested that the severityof bradycardia, degree of peripheral ischemia (especially to muscle)and utilization of arterio-venous shunting are not fixed (Meir andPonganis, 2009; Meir et al., 2008; Ponganis et al., 2009; Ponganis

K. Sato and others

et al., 2007; Stockard et al., 2005). This capacity to alter themagnitude and distribution of blood flow during dives underlies themanagement of O2 stores, and potentially increases the duration ofaerobic metabolism and delays the onset of lactate accumulation.

Lastly, we point out that, despite our emphasis on aerobic diving,exceptionally long dives also occur at sea. The physiologicalcapacity to perform such dives is essential to the success and survivalof emperor penguins. The longest dives are shallow dives, usuallyless than 100m in maximum depth (Kooyman and Kooyman, 1995;Wienecke et al., 2007). In the 27.6min dive in Fig.5, the longestrecorded dive of an emperor penguin, the estimated diving airvolume was 2.4l or 87mlkg–1, providing 17ml O2kg–1 of respiratoryO2, and a total body O2 store of about 63ml O2kg–1. Clearly, somedives are anaerobic, as evidenced by the prolonged post-diverecovery in respiratory rate in Fig.5C, and the 8.4h period beforethis bird began to dive again. Although such dives may be rare,exquisite O2 store management and exceptional hypoxemic andischemic tolerance are essential to survive such incidents. Extremebradycardia, near-complete depletion of the blood O2 store andexceptional anaerobic tolerance undoubtedly contributed to thesuccessful performance of this dive (Meir and Ponganis, 2009; Meiret al., 2008; Ponganis et al., 2009; Ponganis et al., 2007).

PerspectivesAnalysis of surface interval–dive duration relationship confirms thatemperor penguins can perform dives greater in duration than theirADL without prolongation of the surface interval. This occurs bothat sea and at an isolated dive hole, where the 5.6min ADLM hasbeen determined with post-dive blood lactate measurements. Afterconversion of short duration (<2min) dives into part of the post-dive interval, minimum post-dive intervals are still near 1 and 2min,respectively, after 6–7min and 10min dive durations at both sites.

The ability to perform repetitive dives at sea is not afforded bya lower stroke rate. The total number of strokes per dive for divesof equivalent duration is actually higher at sea than at the isolateddive hole. Performance of deep dives at sea is probably facilitated,however, by an increased diving air volume (117mlkg–1) andrespiratory O2 store. Management of this enhanced body O2 storeis probably optimized by cardiovascular adjustments to prolong theduration of aerobic metabolism during dives.

Despite our emphasis on aerobic metabolism during dives,enhanced anaerobic capacity and hypoxemic tolerance undoubtedlyalso contribute to the performance of longer dives (Mill andBaldwin, 1983; Ponganis et al., 2007). This was exemplified by a27.6min dive, recovery from which required 6min before the birdstood up from a prone position, another 20min before it began towalk, and 8.4h before it dived again.

ACKNOWLEDGEMENTSThis work was supported by NSF Grants OPP 0229638, 0538594 and 0944220,and by funds from the Japanese Society for the Promotion of Science(A19255001). We thank the staff of McMurdo Station, especially Fixed WingOperations, for their support, T. Stockard, K. Ponganis, J. Meir, T. Zenteno-Savin,J. St Leger and E. Stockard for their assistance at Penguin Ranch, and Dr N.Miyazaki for his sponsorship (Bio-Logging Science, University of Tokyo) of P.J.P.in Japan to finalize data and manuscript preparation.

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RESEARCH ARTICLE Stroke rates and diving air volumes of … · RESEARCH ARTICLE Stroke rates and diving air volumes of emperor penguins: implications for dive performance Katsufumi